Transcription by an archaeal RNA polymerase is slowed but not blocked by an archaeal nucleosome

Journal of Bacteriology

Volumn 186, Issue 11, 2004, Pages 3492-3498

  Xie, Yunwei ^a   Reeve, John N ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL PROTEIN; HISTONE; PROTEIN HMTA2; RNA POLYMERASE; TATA BINDING PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARCHAEBACTERIUM; ARTICLE; BACTERIAL GENETICS; BACTERIAL GENOME; CHROMATIN; DNA BINDING; DNA STRUCTURE; DNA TEMPLATE; DNA TRANSCRIPTION; ENZYME PURIFICATION; EUKARYOTE; EURYARCHAEOTA; GENE SEQUENCE; GENETIC TRANSCRIPTION; METHANOTHERMUS; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; SEQUENCE HOMOLOGY; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

ARCHAEAL PROTEINS; BASE SEQUENCE; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION REGULATION, ARCHAEAL; METHANOBACTERIACEAE; MOLECULAR SEQUENCE DATA; NUCLEOSOMES; TEMPLATES, GENETIC; TRANSCRIPTION, GENETIC;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; EURYARCHAEOTA; METHANOTHERMOBACTER; METHANOTHERMOBACTER THERMAUTOTROPHICUS; METHANOTHERMUS; PROKARYOTA;

EID: 2442672868     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.11.3492-3498.2004     Document Type: Article

References (65)

1. Adelman, K., A. La Porta, T. J. Santangelo, J. T. Lis, J. W. Roberts, and M. D. Wang. 2002. Single molecule analysis of RNA polymerase elongation reveals uniform kinetic behavior. Proc. Natl. Acad. Sci. USA 99:13538-13543.
2. 2 tetramer-DNA particle. J. Mol. Biol. 291:815-841.
3. Bailey, K. A., C. S. Chow, and J. N. Reeve. 1999. Histone stoichiometry and DNA circularization in archaeal nucleosomes. Nucleic Acids Res. 27:532-536.
4. Bailey, K. A., S. L. Pereira, J. Widom, and J. N. Reeve. 2000. Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution. J. Mol. Biol. 303:25-34.
5. Bailey, K. A., F. Marc, K. Sandman, and J. N. Reeve. 2002. Both DNA and histone fold sequences contribute to archaeal nucleosome stability. J. Biol. Chem. 277:9293-9301.
6. Bednar, J., V. M. Studitsky, S. A. Grigoryev, G. Felsenfeld, and C. L. Woodcock. 1999. The nature of the nucleosomal barrier to transcription: direct observation of paused intermediates by electron cryomicroscopy. Mol. Cell 4:377-386.
7. Bell, S. D., C. H. Botting, B. N. Wardleworth, S. P. Jackson, and M. F. White. 2002. The interaction of Alba, a conserved archaeal chromatin protein, with Sir2 and its regulation by acetylation. Science 296:148-151.
8. Bell, S. D., A. B. Brinkman, J. van der Oost, and S. P. Jackson. 2001. The archaeal TFIIE alpha homologue facilitates transcription initiation by enhancing TATA-box recognition. EMBO Rep. 2:133-138.
9. Bell, S. D., and S. P. Jackson. 2001. Mechanism and regulation of transcription in archaea. Curr. Opin. Microbiol. 4:208-213.
10. Belotserkovskaya, R., S. Oh, V. A. Bondarenko, G. Orphanides, V. M. Studisky, and D. Reinberg. 2003. FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090-1096.
11. Berger, S. L. 2002. Histone modifications in transcription regulation. Curr. Opin. Genet. Dev. 12:142-148.
12. Caetano-Anollés, G., and C. Caetano-Anollés. 2003. An evolutionarily structured universe of protein architecture. Genome Res. 13:1563-1571.
13. Chang, C.-H., and D. S. Luse. 1997. The H3/H4 tetramer blocks transcript elongation by RNA polymerase II in vitro. J. Biol. Chem. 272:23427-23434.
14. 2 tetramers. Arch. Biochem. Biophys. 370:222-230.
15. Cramer, P. 2002. Multisubunit RNA polymerases. Curr. Opin. Struct. Biol. 12:89-97.
16. Darcy, T. J., W. Hausner, D. E. Awery, A. M. Edwards, M. Thomm, and J. N. Reeve. 1999. Methanobacterium thermoautotrophicum RNA polymerase and transcription in vitro. J. Bacteriol. 181:4424-4429.
17. Decanniere, K., A. M. Babu, K. Sandman, J. N. Reeve, and H. Heinemann. 2000. Crystal structures of recombinant histones HMfA and HMfB from the hyperthermophilic archaeon Methanothermus fervidus. J. Mol. Biol. 303:35-47.
18. Dinger, M. E., G. J. Baillie, and D. R. Musgrave. 2000. Growth phase-dependent expression and degradation of histones in the thermophilic archaeon Thermococcus zilligii. Mol. Microbiol. 36:876-885.
19. Edwards, A. M. C. M. Kane, R. A. Young, and R. D. Kornberg. 1991. Two dissociable subunits of yeast RNA polymerase II stimulate the initiation of transcription at a promoter in vitro. J. Biol. Chem. 266:71-75.
20. Hanzelka, B. L., T. J. Darcy, and J. N. Reeve. 2001. TFE, an archaeal transcription factor in Methanobacterium thermoautotrophicum related to eucaryal transcription factor TFIIEα. J. Bacteriol. 183:1813-1818.
21. Hausner, W., U. Lange, and M. Musfeld. 2000. Transcription factor S, a cleavage induction factor of the archaeal RNA polymerase. J. Biol. Chem. 275:12393-12399.
22. Izban, M. G., and D. S. Luse. 1992. Factor-stimulated RNA polymerase II transcribes at physiological elongation rates on naked DNA but very poorly on chromatin templates J. Biol. Chem. 267:13647-13655.
23. Kim, J.-H., W. S. Lane, and D. Reinberg. 2002. Human elongator facilitates RNA polymerase II transcription through chromatin. Proc. Natl. Acad. Sci. USA 99:1241-1246.
24. Kireeva, M. L., W. Walter, V. Tchernajenko, V. Bondarenko, M. Kashlev, and V. M. Studitsky. 2002. Nucleosome remodeling induced by RNA polymerase II: loss of the H2A/H2B dimer during transcription. Mol. Cell 9:541-552.
25. Kirov, N., I. Tsaneva, E. Einbinder, and R. Tsanev. 1992. In vitro transcription through nucleosomes by T7 RNA polymerase. EMBO J. 11:1941-1947.
26. Krypides, N. C., and C. A. Ouzounis. 1999. Transcription in Archaea. Proc. Natl. Acad. Sci. USA 96:8545-8550.
27. Liu, Y. V., D. J. Clark, V. Tchernajenko, M. E. Dahmus, and V. M. Studitsky. 2003. Role of C-terminal domain phosphorylation in RNA polymerase II transcription through the nucleosome. Biopolymers 68:528-538.
28. Lowary, P. T., and J. Widom. 1998. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276:19-42.
29. Luger, K., A. M. Mäder, R. K. Richmond, D. F. Sargent, and T. J. Richmond. 1997. Crystal structure of the nucleosome core particle at 2.8Å resolution. Nature 389:251-260.
30. Luger, K, T. J. Rechsteiner, and T. J. Richmond. 1999. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119:1-16.
31. Luger, K., and T. J. Richmond. 1998. DNA binding within the nucleosome. Curr. Opin. Struct. Biol. 8:33-40.
32. Malik, H. S., and S. Henikoff. 2003. Phylogenetics of the nucleosome. Nat. Struct. Biol. 10:882-891.
33. Marc, F., K. Sandman, R. Lurz, and J. N. Reeve. 2002. Archaeal histone tetramer formation determines DNA affinity, and the direction of DNA supercoiling. J. Biol. Chem. 277:30879-30886.
34. Matsuzaki, H., G. A. Kassavetis, and E. P. Geiduschek. 1994. Analysis of RNA chain elongation and termination by Saccharomyces cerevisiae RNA polymerase III. J. Mol. Biol. 235:1173-1192.
35. Minsky, A., R. Ghirlando, and Z. Reich. 1997. Nucleosomes: a solution to a crowded intracellular environment? J. Theor. Biol. 188:379-385.
36. Narlikar, G. J., H.-Y. Fan, and R. E. Kingston. 2002. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108:475-487.
37. O'Neill, T. E., J. G. Smith, and E. M. Bradbury. 1993. Histone octamer dissociation is not required for transcript elongation through arrays of nucleosome cores by T7 RNA polymerase in vitro. Proc. Natl. Acad. Sci. USA 90:6203-6207.
38. Orphanides, G., and D. Reinberg. 2000. RNA polymerase II elongation through chromatin. Nature 407:471-475.
39. Peränen, J., M. Rikkonen, M. Hyvönen, and L. Kääriäinen. 1996. T7 vectors with modified T7lac promoter for expression of proteins in Escherichia coli. Anal. Biochem. 236:371-373.
40. Pereira, S. L. 1997. An in vivo study of the archaeal histone HMf from the hyperthermophilic methanogen, Methanothermus fervidus. Ph.D. thesis. The Ohio State University, Columbus.
41. Pereira, S. L., R. A. Grayling, R. Lurz, and J. N. Reeve. 1997. Archaeal nucleosomes. Proc. Natl. Acad. Sci. USA 94:12633-12637.
42. Pokholok, D. K., N. M. Hannett, and R. A. Young. 2002. Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol. Cell 9:799-809.
43. Ponting, C. P. 2002. Novel domains and orthologues of eukaryotic transcription elongation factors. Nucleic Acids Res. 30:3643-3652.
44. Protacio, R. U., G. Li, P. T. Lowary, and J. Widom. 2000. Effects of histone tail domains on the rate of transcriptional elongation through a nucleosome. Mol. Cell. Biol. 20:8866-8878.
45. Reeve, J. N. 2003. Archaeal chromatin and transcription. Mol. Microbiol. 48:587-598.
46. Sandman, K., K. Bailey, S. L. Pereira, D. Soares, W.-T. Li, and J. N. Reeve. 2001. Archaeal histones and nucleosomes. Methods Enzymol. 334:116-129.
47. Sandman, K., R. A. Grayling, B. Dobrinski, R. Lurz, and J. N. Reeve. 1994. Growth phase dependent synthesis of histones in the archaeon Methanothermus fervidus. Proc. Natl. Acad. Sci. USA 91:12624-12628.
48. Shioda, M., K. Sugimori, T. Shiroya, and S. Takayanagi. 1989. Nucleosome-like structures associated with chromosomes of the archaebacterium Halobacterium salinarium. J. Bacteriol. 171:4514-4517.
49. Smith, D. R., L. A. Doucette-Stamm, C. DeLoughery, H. Lee, J. Dubois, T. Aldredge, R. Bashirzadeh, D. Blakely, R. Cook, K. Gilbert, D. Harrison, L. Hoang, P. Keagle, W. Lumm, B. Pothier, D. Qiu, R. Spadafora, R. Vicaire, Y. Wang, J. Wierzbowski, R. Gibson, N. Jiwani, A. Caruso, D. Bush, H. Safer, D. Patwell, S. Prabhakar, S. McDougall, G. Shimer, A. Goyal, S. Pietrokovski, G. Church, C. J. Daniels, J. Mao, P. Rice, J. Nölling, and J. N. Reeve. 1997. The complete genome sequence of Methanobacterium thermoautotrophicum strain ΔH: functional analysis and comparative genomics. J. Bacteriol. 179:7135-7155.
50. Soares, D., I. Dahlke, W.-T. Li, K. Sandman, C. Hethke, M. Thomm, and J. N. Reeve. 1998. Archaeal histone stability, DNA binding, and transcription inhibition above 90°C. Extremophiles 2:75-81.
51. Soares, D. J., K. Sandman, and J. N. Reeve. 2000. Mutational analysis of archaeal histone-DNA interactions. J. Mol. Biol. 297:39-47.
52. Spitalny, P., and M. Thomm. 2003. Analysis of the open region and of DNA-protein contacts of archaeal RNA polymerase transcription complexes during transition from initiation to elongation. J. Biol. Chem. 278:30497-30505.
53. Strahl, B. D., and C. D. Allis. 2000. The language of covalent histone modifications. Nature 405:41-45.
54. Studitsky, V. M., G. A. Kassavetis, E. P. Geiduschek, and G. Felsenfeld. 1997. Mechanism of transcription through the nucleosome by eukaryotic RNA polymerase. Science 278:1960-1963.
55. Sullivan, S., D. W. Sink, K. L. Trout, I. Makalowska, P. M. Taylor, A. D. Baxevanis, and D. Landsman. 2002. The histone database. Nucleic Acids. Res. 30:341-342.
56. Svejstrup, J. Q. 2002. Chromatin elongation factors. Curr. Opin. Genet. Dev. 12:156-161.
57. Thåström, A., P. T. Lowary, H. R. Widlund, H. Cao, M. Kubista, and J. Widom. 1999. Sequence motifs and free energies of selected natural and non- natural nucleosome positioning DNA sequences. J. Mol. Biol. 288:213-229.
58. Tomschik, M., M. A. Karymov, J. Zlatanova, and S. H. Leuba. 2001. The archaeal histone-fold protein HMf organizes DNA into bona fide chromatin fibers. Structure 9:1201-1211.
59. Uptain, S. M., C. M. Kane, and M. J. Chamberlin. 1997. Basic mechanisms of transcript elongation and its regulation. Annu. Rev. Biochem. 66:117-172.
60. Waiter, W., M. L. Kireeva, V. M. Studitsky, and M. Kashlev. 2003. Bacterial polymerase and yeast polymerase II use similar mechanisms for transcription through nucleosomes. J. Biol. Chem. 278:36148-36156.
61. Waiter, W., and V. M. Studitsky. 2001. Facilitated transcription through the nucleosome at high ionic strength occurs via a histone octamer transfer mechanism. J. Biol. Chem. 276:29104-29110.
62. Werner, F., and R. O. J. Weinzierl. 2002. A recombinant RNA polymerase II-like enzyme capable of promoter-specific transcription. Mol. Cell 10:635-646.
63. Widlund, H. R., H. Cao, S. Simonsson, E. Magnusson, T. Simonsson, P. E. Nielsen, J. D. Kahn, D. M. Crothers, and M. Kubista. 1997. Identification and characterization of genomic nucleosome-positioning sequences. J. Mol. Biol. 267:807-817.
64. Winkler, G. S., A. Kristjuhan, H. Erdjument-Bromage, P. Tempst, and J. Q. Svetjstrup. 2002. Elongator is a histone H3 and H4 acetyltransferase important for normal histone acetylation levels in vivo. Proc. Natl. Acad. Sci. USA 99:3517-3522.
65. Woychik, N. A., and M. Hampsey. 2002. The RNA polymerase II machinery: structure illuminates function. Cell 108:453-463.